GABAergic Circuits Control Spike-Timing-Dependent Plasticity

Paillé, Vincent; Fino, Élodie; Du, Kai; Morera-Herreras, Teresa; Pérez, Sylvie; Kotaleski, Jeanette Hellgren; Venance, Laurent

doi:10.1523/jneurosci.5796-12.2013

Cited by 122 publications

(175 citation statements)

References 52 publications

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“…The SPN model faithfully reproduces SPN intrinsic membrane properties (SI Appendix, Fig. S1 C and D) (35)(36)(37). In addition, when we simulate somatic membrane potential fluctuations in response to activation of 15 spines (ISI = 1 ms) at distal but not proximal dendrites, a plateau potential can be elicited (Fig.…”

Section: Resultsmentioning

confidence: 68%

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Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Lindroos

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Striatal spiny projection neurons (SPNs) receive convergent excitatory synaptic inputs from the cortex and thalamus. Activation of spatially clustered and temporally synchronized excitatory inputs at the distal dendrites could trigger plateau potentials in SPNs. Such supralinear synaptic integration is crucial for dendritic computation. However, how plateau potentials interact with subsequent excitatory and inhibitory synaptic inputs remains unknown. By combining computational simulation, two-photon imaging, optogenetics, and dualcolor uncaging of glutamate and GABA, we demonstrate that plateau potentials can broaden the spatiotemporal window for integrating excitatory inputs and promote spiking. The temporal window of spiking can be delicately controlled by GABAergic inhibition in a celltype-specific manner. This subtle inhibitory control of plateau potential depends on the location and kinetics of the GABAergic inputs and is achieved by the balance between relief and reestablishment of NMDA receptor Mg 2+ block. These findings represent a mechanism for controlling spatiotemporal synaptic integration in SPNs.O ne of the principal functions of neurons is to integrate excitatory and inhibitory synaptic inputs and transform subthreshold membrane potential fluctuations into suprathreshold spiking activities. Both theoretical and experimental works have proposed that a single neuron can process inputs as a multilayer computational device in which individual dendritic branches function as a computational unit and can generate dendritic spikes or plateau potentials (1-4). In vivo studies have demonstrated that dendritic plateau potentials evoked by coincident inputs can amplify excitatory signals and enhance the capacity of learning and information storage at a specific branch (5-7). However, a majority of the understanding of dendritic computation is based on studies focusing on pyramidal cells of hippocampal and cortical areas. It is relatively less known whether these conclusions apply to the striatal neurons (8).The striatum, the main input nucleus of the basal ganglia, receives convergent glutamatergic inputs from the cortex and thalamus (9-11). The integration of these functionally distinct inputs is critical for fine movement control and action selection (12, 13). The principal neurons in the striatum-spiny projection neurons (SPNs)-display hyperpolarized membrane potentials (∼−80 mV) at rest, often referred to as the "down-state" (14, 15). It is generally believed that coherent cortical inputs can effectively depolarize SPNs and promote membrane potential transitions from a hyperpolarized down-state to a depolarized "up-state" (∼−55 mV), at which point action potentials can be generated (14-16). To achieve this ∼20-to 30-mV state transition, it has been estimated that a large number (hundreds to thousands) of active inputs would be required (14-17). Interestingly, striatal SPNs are capable of producing long-lasting plateau potentials following activation of spatially clustered and temporally synchronized excit...

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Section: Resultsmentioning

confidence: 68%

“…Ion channel kinetics and parameters were tuned to fit the present experimental conditions (SI Appendix, Fig. S1) and previously published data (35)(36)(37). This is further motivated because SPN dendrites are too thin to be directly accessed using patch-clamp techniques.…”

Section: Resultsmentioning

confidence: 99%

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Lindroos

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Previous studies have shown that using an agonist for CBR1 (WIN 55,212-2) (44) or mGluR5 (42,45) modulators in HD mouse models ameliorates several alterations associated with corticostriatal dysfunction. Alterations in excitatory-inhibitory (E-I) balance can also deregulate corticostriatal plasticity (46). Changes in inhibitory (47,48) and excitatory (14,17) inputs to different striatal neurons (MSN-D1 and MSN-D2, fast-spiking interneurons, and persistent low-threshold interneurons) have been observed in BACHD (at both 2 and 12 mo of age) (47) and other mouse models of HD, thereby suggesting another mechanism to explain the alterations in corticostriatal plasticity.…”

Section: Discussionmentioning

confidence: 99%

Selective expression of mutant huntingtin during development recapitulates characteristic features of Huntington’s disease

Molero

Arteaga-Bracho

Chen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

115

100

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Recent studies have identified impairments in neural induction and in striatal and cortical neurogenesis in Huntington’s disease (HD) knock-in mouse models and associated embryonic stem cell lines. However, the potential role of these developmental alterations for HD pathogenesis and progression is currently unknown. To address this issue, we used BACHD:CAG-CreERT2 mice, which carry mutant huntingtin (mHtt) modified to harbor a floxed exon 1 containing the pathogenic polyglutamine expansion (Q97). Upon tamoxifen administration at postnatal day 21, the floxed mHtt-exon1 was removed and mHtt expression was terminated (Q97CRE). These conditional mice displayed similar profiles of impairments to those mice expressing mHtt throughout life: (i) striatal neurodegeneration, (ii) early vulnerability to NMDA-mediated excitotoxicity, (iii) impairments in motor coordination, (iv) temporally distinct abnormalities in striatal electrophysiological activity, and (v) altered corticostriatal functional connectivity and plasticity. These findings strongly suggest that developmental aberrations may play important roles in HD pathogenesis and progression.

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“…Specifically, corticostriatal synapses onto medium spiny neurons are potentiated when presynaptic release precedes postsynaptic depolarization (Hebbian LTP) only when GABA A is blocked; when GABA A is not blocked, pre-post pairing is depressing, and LTP is instead evoked when postsynaptic depolarization preceded presynaptic release (antiHebbian) (Fino et al 2010). Several mechanisms have been proposed to account for reversal of STDP by GABA A , such as altered ratio of NMDA to L-type calcium influx in dendrites (Paille et al 2013) or Hebbian potentiation of feed-forward inhibition (Fino et al 2008). Alternatively, increased dopamine release may be responsible for switching STDP direction (Shen et al 2008;Shindou et al 2011), since GABA A antagonists increase activity-dependent intrastriatal dopamine release (Juranyi et al 2003).…”

Section: Discussionmentioning

confidence: 99%

“…STDP protocols employ lower, more reasonable frequencies to pair postsynaptic action potentials with precisely timed presynaptic stimulation in normal Mg 2ϩ , and in these regards STDP is more physiological than HFS. STDP can be used to evoke LTP or LTD as desired based on the relative timing of activity across the synapse (Fino et al 2005) and whether GABA A receptors are blocked (Fino et al 2010;Paille et al 2013), but, as with HFS stimulation, STDP LTP is not consistently observed (Shindou et al 2011). Because diverse induction paradigms invoke plasticity by way of distinct molecular mechanisms (Asrar et al 2009;Lerner and Kreitzer 2012;Petersen et al 2003;Ronesi and Lovinger 2004), it would be ideal to use normal magnesium solutions in combination with physiological, learning-like activity to induce longlasting plasticity for the purpose of examining subcellular learning mechanisms.…”

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confidence: 99%

Sensitivity to theta-burst timing permits LTP in dorsal striatal adult brain slice

Hawes

Gillani

Evans

et al. 2013

Journal of Neurophysiology

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Long-term potentiation (LTP) of excitatory afferents to the dorsal striatum likely occurs with learning to encode new skills and habits, yet corticostriatal LTP is challenging to evoke reliably in brain slice under physiological conditions. Here we test the hypothesis that stimulating striatal afferents with theta-burst timing, similar to recently reported in vivo temporal patterns corresponding to learning, evokes LTP. Recording from adult mouse brain slice extracellularly in 1 mM Mg 2ϩ , we find LTP in dorsomedial and dorsolateral striatum is preferentially evoked by certain theta-burst patterns. In particular, we demonstrate that greater LTP is produced using moderate intraburst and high thetarange frequencies, and that pauses separating bursts of stimuli are critical for LTP induction. By altering temporal pattern alone, we illustrate the importance of burst-patterning for LTP induction and demonstrate that corticostriatal long-term depression is evoked in the same preparation. In accord with prior studies, LTP is greatest in dorsomedial striatum and relies on N-methyl-D-aspartate receptors. We also demonstrate a requirement for both G q -and G s/olf -coupled pathways, as well as several kinases associated with memory storage: PKC, PKA, and ERK. Our data build on previous reports of activitydirected plasticity by identifying effective values for distinct temporal parameters in variants of theta-burst LTP induction paradigms. We conclude that those variants which best match reports of striatal activity during learning behavior are most successful in evoking dorsal striatal LTP in adult brain slice without altering artificial cerebrospinal fluid. Future application of this approach will enable diverse investigations of plasticity serving striatal-based learning.

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GABAergic Circuits Control Spike-Timing-Dependent Plasticity

Cited by 122 publications

References 52 publications

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Selective expression of mutant huntingtin during development recapitulates characteristic features of Huntington’s disease

Sensitivity to theta-burst timing permits LTP in dorsal striatal adult brain slice

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